Diesel exhaust particles impair endothelial progenitor cells, compromise endothelial integrity, reduce neoangiogenesis, and increase atherogenesis in mice

Cardiovascular Toxicology

Volumn 13, Issue 3, 2013, Pages 290-300

  Pöss, Janine ^a   Lorenz, Dominik ^a   Werner, Christian ^a   Pavlikova, Valerie ^a   Gensch, Christoph ^a   Speer, Thimoteus ^a   Alessandrini, Francesca ^b   Berezowski, Vincent ^c,d   Kuntz, Mélanie ^c,d   Mempel, Martin ^e   Endres, Matthias ^f   Böhm, Michael ^a   Laufs, Ulrich ^a  

^a SAARLAND UNIVERSITY   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c UNIV LILLE   (France)

^d UNIVERSITÉ D'ARTOIS   (France)

^e UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^f CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Basic science; Diesel exhaust particles; Endothelial progenitor cells

Indexed keywords

APOLIPOPROTEIN E; DIESEL FUEL; GLUCOSE; LECTIN; OXYGEN; REACTIVE OXYGEN METABOLITE; SUPEROXIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA SINUS; APOPTOSIS; ARTICLE; ATHEROGENESIS; ATHEROSCLEROTIC PLAQUE; BLOOD BRAIN BARRIER; BLOOD VESSEL INJURY; BRONCHUS; CELL COUNT; CELL FUNCTION; CELL MIGRATION; COLONY FORMING UNIT; CONTROLLED STUDY; ENDOTHELIAL PROGENITOR CELL; ENDOTHELIUM; EXHAUST GAS; EXPOSURE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LUNG INTERSTITIUM; MOUSE; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; PARTICULATE MATTER; PATHOPHYSIOLOGY; PREDICTION; PRIORITY JOURNAL; VASCULAR ENDOTHELIUM;

MUS;

AIR POLLUTANTS; ANIMALS; ANOXIA; APOLIPOPROTEINS E; APOPTOSIS; ATHEROSCLEROSIS; BLOOD-BRAIN BARRIER; CELL MOVEMENT; CELL SEPARATION; ELECTRON SPIN RESONANCE SPECTROSCOPY; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; GLUCOSE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEOVASCULARIZATION, PHYSIOLOGIC; PARTICULATE MATTER; SPLEEN; STEM CELLS; SUPEROXIDES; VEHICLE EMISSIONS;

EID: 84884290922     PISSN: 15307905     EISSN: 15590259     Source Type: Journal    
DOI: 10.1007/s12012-013-9208-0     Document Type: Article

References (58)

1. Asahara, T., Murohara, T., Sullivan, A., Silver, M., van der Zee, R., Li, T., et al. (1997). Isolation of putative progenitor endothelial cells for angiogenesis. Science, 275, 964-967.
2. Aicher, A., Heeschen, C., Mildner-Rihm, C., Urbich, C., Ihling, C., Technau-Ihling, K., et al. (2003). Essential role of endothelial nitric oxide synthase for mobilization of stem and progenitor cells. Nature Medicine, 9, 1370-1376.
3. Dimmeler, S., Aicher, A., Vasa, M., Mildner-Rihm, C., Adler, K., Tiemann, M., et al. (2001). HMG-CoA reductase inhibitors (statins) increase endothelial progenitor cells via the PI 3-kinase/Akt pathway. Journal of Clinical Investigation, 108, 391-397.
4. Hill, J. M., Zalos, G., Halcox, J. P., Schenke, W. H., Waclawiw, M. A., Quyyumi, A. A., et al. (2003). Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. New England Journal of Medicine, 348, 593-600.
5. Schachinger, V., Assmus, B., Honold, J., Lehmann, R., Hofmann, W. K., Martin, H., et al. (2006). Normalization of coronary blood flow in the infarct-related artery after intracoronary progenitor cell therapy: Intracoronary Doppler substudy of the TOPCARE-AMI trial. Clinical Research Cardiology, 95, 13-22.
6. Strehlow, K., Werner, N., Berweiler, J., Link, A., Dirnagl, U., Priller, J., et al. (2003). Estrogen increases bone marrow-derived endothelial progenitor cell production and diminishes neointima formation. Circulation, 107, 3059-3065.
7. Walter, D. H., Rittig, K., Bahlmann, F. H., Kirchmair, R., Silver, M., Murayama, T., et al. (2002). Statin therapy accelerates reendothelialization: A novel effect involving mobilization and incorporation of bone marrow-derived endothelial progenitor cells. Circulation, 105, 3017-3024.
8. Werner, N., Junk, S., Laufs, U., Link, A., Walenta, K., Böhm, M., et al. (2003). Intravenous transfusion of endothelial progenitor cells reduces neointima formation after vascular injury. Circulation Research, 93, e17-e24.
9. Schroder, K., Kohnen, A., Aicher, A., Liehn, E. A., Buchse, T., Stein, S., et al. (2009). NADPH oxidase Nox2 is required for hypoxia-induced mobilization of endothelial progenitor cells. Circulation Research, 105, 537-544.
10. Steinmetz, M., Brouwers, C., Nickenig, G., & Wassmann, S. (2010). Synergistic effects of telmisartan and simvastatin on endothelial progenitor cells. Journal of Cellular and Molecular Medicine, 14(6B), 1645-1656.
11. Gensch, C., Clever, Y. P., Werner, C., Hanhoun, M., Böhm, M., & Laufs, U. (2007). The PPAR-gamma agonist pioglitazone increases neoangiogenesis and prevents apoptosis of endothelial progenitor cells. Atherosclerosis, 192, 67-74.
12. Schuh, A., Liehn, E. A., Sasse, A., Hristov, M., Sobota, R., Kelm, M., et al. (2008). Transplantation of endothelial progenitor cells improves neovascularization and left ventricular function after myocardial infarction in a rat model. Basic Research in Cardiology, 103, 69-77.
13. Schmidt-Lucke, C., Rossig, L., Fichtlscherer, S., Vasa, M., Britten, M., Kamper, U., et al. (2005). Reduced number of circulating endothelial progenitor cells predicts future cardiovascular events: Proof of concept for the clinical importance of endogenous vascular repair. Circulation, 111, 2981-2987.
14. Werner, N., Kosiol, S., Schiegl, T., Ahlers, P., Walenta, K., Link, A., et al. (2005). Circulating endothelial progenitor cells and cardiovascular outcomes. New England Journal of Medicine, 353, 999-1007.
15. Fadini, G. P., Sartore, S., Albiero, M., Baesso, I., Murphy, E., Menegolo, M., et al. (2006). Number and function of endothelial progenitor cells as a marker of severity for diabetic vasculopathy. Arteriosclerosis, Thrombosis, and Vascular Biology, 26, 2140-2146.
16. Ii, M., Takenaka, H., Asai, J., Ibusuki, K., Mizukami, Y., Maruyama, K., et al. (2006). Endothelial progenitor thrombospondin-1 mediates diabetes-induced delay in reendothelialization following arterial injury. Circulation Research, 98, 697-704.
17. Shintani, S., Murohara, T., Ikeda, H., Ueno, T., Honma, T., Katoh, A., et al. (2001). Mobilization of endothelial progenitor cells in patients with acute myocardial infarction. Circulation, 103, 2776-2779.
18. Tepper, O. M., Galiano, R. D., Capla, J. M., Kalka, C., Gagne, P. J., Jacobowitz, G. R., et al. (2002). Human endothelial progenitor cells from type II diabetics exhibit impaired proliferation, adhesion, and incorporation into vascular structures. Circulation, 106, 2781-2786.
19. Vasa, M., Fichtlscherer, S., Aicher, A., Adler, K., Urbich, C., Martin, H., et al. (2001). Number and migratory activity of circulating endothelial progenitor cells inversely correlate with risk factors for coronary artery disease. Circulation Research, 89, E1-E7.
20. Werner, N., Priller, J., Laufs, U., Endres, M., Böhm, M., Dirnagl, U., et al. (2002). Bone marrow-derived progenitor cells modulate vascular reendothelialization and neointimal formation: Effect of 3-hydroxy-3- methylglutaryl coenzyme a reductase inhibition. Arteriosclerosis, Thrombosis, and Vascular Biology, 22, 1567-1572.
21. Kleinbongard, P., & Weber, A. A. (2008). Impaired interaction between platelets and endothelial progenitor cells in diabetic patients. Basic Research in Cardiology, 103, 569-571.
22. Dernbach, E., Randriamboavonjy, V., Fleming, I., Zeiher, A. M., Dimmeler, S., & Urbich, C. (2008). Impaired interaction of platelets with endothelial progenitor cells in patients with cardiovascular risk factors. Basic Research in Cardiology, 103, 572-581.
23. Friedrich, E. B., Werner, C., Walenta, K., Böhm, M., & Scheller, B. (2009). Role of extracellular signal-regulated kinase for endothelial progenitor cell dysfunction in coronary artery disease. Basic Research in Cardiology, 104, 613-620.
24. Keymel, S., Kalka, C., Rassaf, T., Yeghiazarians, Y., Kelm, M., & Heiss, C. (2008). Impaired endothelial progenitor cell function predicts age-dependent carotid intimal thickening. Basic Research in Cardiology, 103, 582-586.
25. Fadini, G. P., Albiero, M., Menegazzo, L., Boscaro, E., Agostini, C., de Kreutzenberg, S. V., et al. (2012). Procalcific phenotypic drift of circulating progenitor cells in type 2 diabetes with coronary artery disease. Experimental Diabetes Research, 2012, 921685.
26. Adams, V., Lenk, K., Linke, A., Lenz, D., Erbs, S., Sandri, M., et al. (2004). Increase of circulating endothelial progenitor cells in patients with coronary artery disease after exercise-induced ischemia. Arteriosclerosis, Thrombosis, and Vascular Biology, 24, 684-690.
27. Laufs, U., Werner, N., Link, A., Endres, M., Wassmann, S., Jurgens, K., et al. (2004). Physical training increases endothelial progenitor cells, inhibits neointima formation, and enhances angiogenesis. Circulation, 109, 220-226.
28. Bhatnagar, A. (2006). Environmental cardiology: Studying mechanistic links between pollution and heart disease. Circulation Research, 99, 692-705.
29. Brook, R. D., Rajagopalan, S., Pope, C. A., 3rd, Brook, J. R., Bhatnagar, A., Diez-Roux, A. V., et al. (2010). Particulate matter air pollution and cardiovascular disease: An update to the scientific statement from the American Heart Association. Circulation, 121, 2331-2378.
30. Pope, C. A., 3rd, Ezzati, M., & Dockery, D. W. (2009). Fine-particulate air pollution and life expectancy in the United States. New England Journal of Medicine, 360, 376-386.
31. Mills, N. L., Tornqvist, H., Gonzalez, M. C., Vink, E., Robinson, S. D., Soderberg, S., et al. (2007). Ischemic and thrombotic effects of dilute diesel-exhaust inhalation in men with coronary heart disease. New England Journal of Medicine, 357, 1075-1082.
32. Sun, Q., Wang, A., Jin, X., Natanzon, A., Duquaine, D., Brook, R. D., et al. (2005). Long-term air pollution exposure and acceleration of atherosclerosis and vascular inflammation in an animal model. The Journal of the American Medical Association, 294, 3003-3010.
33. O'Toole, T. E., Hellmann, J., Wheat, L., Haberzettl, P., Lee, J., Conklin, D. J., et al. (2010). Episodic exposure to fine particulate air pollution decreases circulating levels of endothelial progenitor cells. Circulation Research, 107, 200-203.
34. Kampfrath, T., Maiseyeu, A., Ying, Z., Shah, Z., Deiuliis, J. A., Xu, X., et al. (2011). Chronic fine particulate matter exposure induces systemic vascular dysfunction via NADPH oxidase and TLR4 pathways. Circulation Research, 108, 716-726.
35. National Insitute of Standards and Technology. (2006). SRM 1650b, Diesel Particulate Matter. Gaithersburg, MD: Department of Commerce.
36. Laufs, U., Urhausen, A., Werner, N., Scharhag, J., Heitz, A., Kissner, G., et al. (2005). Running exercise of different duration and intensity: Effect on endothelial progenitor cells in healthy subjects. European Journal of Cardiovascular Prevention and Rehabilitaion, 12, 407-414.
37. Sorrentino, S. A., Doerries, C., Manes, C., Speer, T., Dessy, C., Lobysheva, I., et al. (2011). Nebivolol exerts beneficial effects on endothelial function, early endothelial progenitor cells, myocardial neovascularization, and left ventricular dysfunction early after myocardial infarction beyond conventional beta1-blockade. Journal of the American College of Cardiology, 57, 601-611.
38. Winnik, S., Lohmann, C., Richter, E. K., Schafer, N., Song, W. L., Leiber, F., et al. (2011). Dietary alpha-linolenic acid diminishes experimental atherogenesis and restricts T cell-driven inflammation. European Heart Journal, 32, 2573-2584.
39. Werner, N., Wassmann, S., Ahlers, P., Kosiol, S., & Nickenig, G. (2006). Circulating CD31 +/annexin V + apoptotic microparticles correlate with coronary endothelial function in patients with coronary artery disease. Arteriosclerosis, Thrombosis, and Vascular Biology, 26, 112-116.
40. Meresse, S., Dehouck, M. P., Delorme, P., Bensaid, M., Tauber, J. P., Delbart, C., et al. (1989). Bovine brain endothelial cells express tight junctions and monoamine oxidase activity in long-term culture. Journal of Neurochemistry, 53, 1363-1371.
41. Dehouck, M. P., Meresse, S., Delorme, P., Fruchart, J. C., & Cecchelli, R. (1990). An easier, reproducible, and mass-production method to study the blood-brain barrier in vitro. Journal of Neurochemistry, 54, 1798-1801.
42. Dehouck, M. P., Jolliet-Riant, P., Bree, F., Fruchart, J. C., Cecchelli, R., & Tillement, J. P. (1992). Drug transfer across the blood-brain barrier: Correlation between in vitro and in vivo models. Journal of Neurochemistry, 58, 1790-1797.
43. Brillault, J., Berezowski, V., Cecchelli, R., & Dehouck, M. P. (2002). Intercommunications between brain capillary endothelial cells and glial cells increase the transcellular permeability of the blood-brain barrier during ischaemia. Journal of Neurochemistry, 83, 807-817.
44. Seeger, F. H., Sedding, D., Langheinrich, A. C., Haendeler, J., Zeiher, A. M., & Dimmeler, S. (2010). Inhibition of the p38 MAP kinase in vivo improves number and functional activity of vasculogenic cells and reduces atherosclerotic disease progression. Basic Research in Cardiology, 105, 389-397.
45. Rauscher, F. M., Goldschmidt-Clermont, P. J., Davis, B. H., Wang, T., Gregg, D., Ramaswami, P., et al. (2003). Aging, progenitor cell exhaustion, and atherosclerosis. Circulation, 108, 457-463.
46. Peters, A., von Klot, S., Heier, M., Trentinaglia, I., Hormann, A., Wichmann, H. E., et al. (2004). Exposure to traffic and the onset of myocardial infarction. New England Journal of Medicine, 351, 1721-1730.
47. Peters, A., & Pope, C. A., 3rd. (2002). Cardiopulmonary mortality and air pollution. Lancet, 360, 1184-1185.
48. Harrison, D., Griendling, K. K., Landmesser, U., Hornig, B., & Drexler, H. (2003). Role of oxidative stress in atherosclerosis. American Journal of Cardiology, 91, 7A-11A.
49. Imanishi, T., Hano, T., & Nishio, I. (2005). Angiotensin II accelerates endothelial progenitor cell senescence through induction of oxidative stress. Journal of Hypertension, 23, 97-104.
50. Thum, T., Fraccarollo, D., Thum, S., Schultheiss, M., Daiber, A., Wenzel, P., et al. (2007). Differential effects of organic nitrates on endothelial progenitor cells are determined by oxidative stress. Arteriosclerosis, Thrombosis, and Vascular Biology, 27, 748-754.
51. Imanishi, T., Tsujioka, H., Ikejima, H., Kuroi, A., Takarada, S., Kitabata, H., et al. (2008). Renin inhibitor aliskiren improves impaired nitric oxide bioavailability and protects against atherosclerotic changes. Hypertension, 52, 563-572.
52. Lu, H., Rateri, D. L., Feldman, D. L., Jr, R. J., Fukamizu, A., Ishida, J., et al. (2008). Renin inhibition reduces hypercholesterolemia-induced atherosclerosis in mice. Journal of Clinical Investigation, 118, 984-993.
53. Nussberger, J., Aubert, J. F., Bouzourene, K., Pellegrin, M., Hayoz, D., & Mazzolai, L. (2008). Renin inhibition by aliskiren prevents atherosclerosis progression: Comparison with irbesartan, atenolol, and amlodipine. Hypertension, 51, 1306-1311.
54. Mutlu, G. M., Green, D., Bellmeyer, A., Baker, C. M., Burgess, Z., Rajamannan, N., et al. (2007). Ambient particulate matter accelerates coagulation via an IL-6-dependent pathway. Journal of Clinical Investigation, 117, 2952-2961.
55. van Eeden, S. F., Tan, W. C., Suwa, T., Mukae, H., Terashima, T., Fujii, T., et al. (2001). Cytokines involved in the systemic inflammatory response induced by exposure to particulate matter air pollutants (PM(10)). American Journal of Respiratory and Critical Care Medicine, 164, 826-830.
56. Kondo, T., Hayashi, M., Takeshita, K., Numaguchi, Y., Kobayashi, K., Iino, S., et al. (2004). Smoking cessation rapidly increases circulating progenitor cells in peripheral blood in chronic smokers. Arteriosclerosis, Thrombosis, and Vascular Biology, 24, 1442-1447.
57. DeLorme, M. P., & Moss, O. R. (2002). Pulmonary function assessment by whole-body plethysmography in restrained versus unrestrained mice. Journal of Pharmacological and Toxicological Methods, 47, 1-10.
58. Irvin, C. G., & Bates, J. H. (2003). Measuring the lung function in the mouse: The challenge of size. Respiratory Research, 4, 4.